skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Structural and Mechanistic Insights into Hemoglobin-catalyzed Hydrogen Sulfide Oxidation and the Fate of Polysulfide Products

Journal Article · · Journal of Biological Chemistry
 [1];  [1];  [1];  [2];  [1];  [1]
  1. Univ. of Michigan Medical School, Ann Arbor, MI (United States)
  2. Univ. of Nebraska, Lincoln, NE (United States)

Hydrogen sulfide is a cardioprotective signaling molecule but is toxic at elevated concentrations. Red blood cells can synthesize H2S but, lacking organelles, cannot dispose of H2S via the mitochondrial sulfide oxidation pathway. We have recently shown that at high sulfide concentrations, ferric hemoglobin oxidizes H2S to a mixture of thiosulfate and iron-bound polysulfides in which the latter species predominates. Here, we report the crystal structure of human hemoglobin containing low spin ferric sulfide, the first intermediate in heme-catalyzed sulfide oxidation. Here, the structure provides molecular insights into why sulfide is susceptible to oxidation in human hemoglobin but is stabilized against it in HbI, a specialized sulfide-carrying hemoglobin from a mollusk adapted to life in a sulfide-rich environment. We have also captured a second sulfide bound at a postulated ligand entry/exit site in the α-subunit of hemoglobin, which, to the best of our knowledge, represents the first direct evidence for this site being used to access the heme iron. Hydrodisulfide, a postulated intermediate at the junction between thiosulfate and polysulfide formation, coordinates ferric hemoglobin and, in the presence of air, generated thiosulfate. At low sulfide/heme iron ratios, the product distribution between thiosulfate and iron-bound polysulfides was approximately equal. The iron-bound polysulfides were unstable at physiological glutathione concentrations and were reduced with concomitant formation of glutathione persulfide, glutathione disulfide, and H2S. Hence, although polysulfides are unlikely to be stable in the reducing intracellular milieu, glutathione persulfide could serve as a persulfide donor for protein persulfidation, a posttranslational modification by which H2S is postulated to signal.

Research Organization:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Organization:
National Inst. of Health
Grant/Contract Number:
GM112455; DK111465
OSTI ID:
1351356
Journal Information:
Journal of Biological Chemistry, Vol. 292, Issue 13; ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular BiologyCopyright Statement
Country of Publication:
United States
Language:
ENGLISH
Citation Metrics:
Cited by: 40 works
Citation information provided by
Web of Science

References (38)

Hydrogen Sulfide and Hemeproteins: Knowledge and Mysteries journal July 2011
H2S Signals Through Protein S-Sulfhydration journal November 2009
Pattern of cavities in globins: The case of human hemoglobin journal December 2009
Hydrogen Sulfide Oxidation by Myoglobin journal June 2016
Biosynthesis and Reactivity of Cysteine Persulfides in Signaling journal December 2015
Relative Contributions of Cystathionine β-Synthase and γ-Cystathionase to H 2 S Biogenesis via Alternative Trans-sulfuration Reactions journal June 2009
Glutathione Synthesis and Turnover in the Human Erythrocyte: ALIGNMENT OF A MODEL BASED ON DETAILED ENZYME KINETICS WITH EXPERIMENTAL DATA journal May 2010
Averaged kick maps: less noise, more signal…and probably less bias journal August 2009
Trisulfide Modification Impacts the Reduction Step in Antibody–Drug Conjugation Process journal June 2013
Rapid Reaction of Hydrogen Sulfide with the Neutrophil Oxidant Hypochlorous Acid to Generate Polysulfides journal October 2010
The Nitrite Anion Binds to Human Hemoglobin via the Uncommon O -Nitrito Mode journal August 2008
The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration journal June 2009
Features and development of Coot journal March 2010
Human Methionine Synthase Reductase, a Soluble P-450 Reductase-like Dual Flavoprotein, Is Sufficient for NADPH-dependent Methionine Synthase Activation journal July 2001
Structural and Functional Insights into Sulfide:Quinone Oxidoreductase , journal June 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Sulfide Oxidation by a Noncanonical Pathway in Red Blood Cells Generates Thiosulfate and Polysulfides journal February 2015
H 2 S Biogenesis by Human Cystathionine γ-Lyase Leads to the Novel Sulfur Metabolites Lanthionine and Homolanthionine and Is Responsive to the Grade of Hyperhomocysteinemia journal March 2009
Polysulfides Link H 2 S to Protein Thiol Oxidation journal November 2013
Sulfide-hemoglobin interactions in the sulfide-tolerant salt marsh resident, the California killifish Fundulus parvipinnis journal November 1992
Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria: Reactions of mitochondrial sulfide oxidation journal June 2008
An Atomistic View on Human Hemoglobin Carbon Monoxide Migration Processes journal February 2012
Organization of the Human Mitochondrial Hydrogen Sulfide Oxidation Pathway journal September 2014
Using a functional enzyme model to understand the chemistry behind hydrogen sulfide induced hibernation journal December 2009
O 2 and Water Migration Pathways between the Solvent and Heme Pockets of Hemoglobin with Open and Closed Conformations of the Distal HisE7 journal August 2015
Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling journal April 2014
Quaternary-Linked Changes in Structure and Dynamics That Modulate O 2 Migration within Hemoglobin’s Gas Diffusion Tunnels journal August 2015
XDS journal January 2010
Biogenesis of reactive sulfur species for signaling by hydrogen sulfide oxidation pathways journal June 2015
Signaling of Hydrogen Sulfide and Polysulfides journal February 2015
Kinetics of oxidation of aqueous sulfide by oxygen journal June 1972
Phaser crystallographic software journal July 2007
Enzymatic Formation of Polysulfides from Mercaptopyruvate journal August 1959
Hemoglobins of the Lucina pectinata/bacteria symbiosis. I. Molecular properties, kinetics and equilibria of reactions with ligands. journal September 1990
Hemoglobins of the Lucina pectinata/bacteria symbiosis. II. An electron paramagnetic resonance and optical spectral study of the ferric proteins. journal September 1990
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome journal December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation journal February 2021
PHENIX: a comprehensive Python-based system for macromolecular structure solution. text January 2010

Cited By (13)

Mechanism-based inhibition of human persulfide dioxygenase by γ-glutamyl-homocysteinyl-glycine journal July 2018
Hydrogen Sulfide and Persulfides Oxidation by Biologically Relevant Oxidizing Species journal February 2019
Hydrogen Sulfide: Emerging Role in Bladder, Kidney, and Prostate Malignancies journal November 2019
3-Mercaptopyruvate sulfurtransferase produces potential redox regulators cysteine- and glutathione-persulfide (Cys-SSH and GSSH) together with signaling molecules H2S2, H2S3 and H2S journal September 2017
Hydrogen Sulfide Biochemistry and Interplay with Other Gaseous Mediators in Mammalian Physiology journal June 2018
Persulfides, at the crossroads between hydrogen sulfide and thiols journal February 2020
Uremic Toxin Lanthionine Interferes with the Transsulfuration Pathway, Angiogenetic Signaling and Increases Intracellular Calcium journal May 2019
Hemoglobin-Catalyzed Synthesis of Indolizines Under Mild Conditions: Hemoglobin-Catalyzed Synthesis of Indolizines Under Mild Conditions journal December 2019
Speciation of reactive sulfur species and their reactions with alkylating agents: do we have any clue about what is present inside the cell?: Speciation of reactive sulfur species journal August 2018
Non-enzymatic hydrogen sulfide production from cysteine in blood is catalyzed by iron and vitamin B6 journal May 2019
International Union of Basic and Clinical Pharmacology. CII: Pharmacological Modulation of H 2 S Levels: H 2 S Donors and H 2 S Biosynthesis Inhibitors journal September 2017
Emerging pharmacological tools to control hydrogen sulfide signaling in critical illness journal January 2020
3-Mercaptopyruvate sulfurtransferase produces potential redox regulators cysteineand glutathione-persulfide (Cys-SSH and GSSH) together with signaling molecules H2S2, H2S3 and H2S journal January 2018

Similar Records

Structural and biochemical analyses indicate that a bacterial persulfide dioxygenase–rhodanese fusion protein functions in sulfur assimilation
Journal Article · Thu Jul 06 00:00:00 EDT 2017 · Journal of Biological Chemistry · OSTI ID:1351356

Lucina pectinata oxyhemoglobin (II-III) heterodimer pH susceptibility
Journal Article · Sat Mar 07 00:00:00 EST 2020 · Journal of Inorganic Biochemistry · OSTI ID:1351356

Homolytic cleavage of both heme-bound hydrogen peroxide and hydrogen sulfide leads to the formation of sulfheme
Journal Article · Wed Jun 29 00:00:00 EDT 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1351356